Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH

8-oxo-7,8-dihydroguanine (OG) is one of the most abundant oxidative lesions in the genome and is associated with genome instability. Its mutagenic potential is counteracted by a concerted action of 8-oxoguanine DNA glycosylase (OGG1) and mutY homolog DNA glycosylase (MUTYH). It has been suggested th...

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Main Authors: Tobias Obermann, Teri Sakshaug, Vishnu Vignesh Kanagaraj, Andreas Abentung, Mirta Mittelstedt Leal de Sousa, Lars Hagen, Antonio Sarno, Magnar Bjørås, Katja Scheffler
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Redox Biology
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231724004397
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author Tobias Obermann
Teri Sakshaug
Vishnu Vignesh Kanagaraj
Andreas Abentung
Mirta Mittelstedt Leal de Sousa
Lars Hagen
Antonio Sarno
Magnar Bjørås
Katja Scheffler
author_facet Tobias Obermann
Teri Sakshaug
Vishnu Vignesh Kanagaraj
Andreas Abentung
Mirta Mittelstedt Leal de Sousa
Lars Hagen
Antonio Sarno
Magnar Bjørås
Katja Scheffler
author_sort Tobias Obermann
collection DOAJ
description 8-oxo-7,8-dihydroguanine (OG) is one of the most abundant oxidative lesions in the genome and is associated with genome instability. Its mutagenic potential is counteracted by a concerted action of 8-oxoguanine DNA glycosylase (OGG1) and mutY homolog DNA glycosylase (MUTYH). It has been suggested that OG and its repair has epigenetic-like properties and mediates transcription, but genome-wide evidence of this interdependence is lacking. Here, we applied an improved OG-sequencing approach reducing artificial background oxidation and RNA-sequencing to correlate genome-wide distribution of OG with gene transcription in OGG1 and/or MUTYH-deficient cells. Our data identified moderate enrichment of OG in the genome that is mainly dependent on the genomic context and not affected by DNA glycosylase-initiated repair. Interestingly, no association was found between genomic OG deposition and gene expression changes upon loss of OGG1 and MUTYH. Regardless of DNA glycosylase activity, OG in promoter regions correlated with expression of genes related to metabolic processes and damage response pathways indicating that OG functions as a cellular stress sensor to regulate transcription. Our work provides novel insights into the mechanism underlying transcriptional regulation by OG and DNA glycosylases OGG1 and MUTYH and suggests that oxidative DNA damage accumulation and its repair utilize different pathways.
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spelling doaj-art-aae87b07b5444177b8163c2a99b4572a2025-01-14T04:12:09ZengElsevierRedox Biology2213-23172025-02-0179103461Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYHTobias Obermann0Teri Sakshaug1Vishnu Vignesh Kanagaraj2Andreas Abentung3Mirta Mittelstedt Leal de Sousa4Lars Hagen5Antonio Sarno6Magnar Bjørås7Katja Scheffler8Department of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491, Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, Norway; Department of Neurology and Clinical Neurophysiology, University Hospital of Trondheim, 7006, Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, Norway; Proteomics and Modomics Experimental Core (PROMEC), NTNU and the Central Norway Regional Health Authority, N-7491, Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, Norway; Proteomics and Modomics Experimental Core (PROMEC), NTNU and the Central Norway Regional Health Authority, N-7491, Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, NorwayDepartment of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491 Trondheim, Norway; Centre for Embryology and Healthy Development, University of Oslo, Oslo, 0373, Norway; Department of Microbiology, Oslo University Hospital and University of Oslo, Oslo, 0424, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491, Trondheim, Norway; Department of Neurology and Clinical Neurophysiology, University Hospital of Trondheim, 7006, Trondheim, Norway; Corresponding author. Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, 7491, Trondheim, Norway.8-oxo-7,8-dihydroguanine (OG) is one of the most abundant oxidative lesions in the genome and is associated with genome instability. Its mutagenic potential is counteracted by a concerted action of 8-oxoguanine DNA glycosylase (OGG1) and mutY homolog DNA glycosylase (MUTYH). It has been suggested that OG and its repair has epigenetic-like properties and mediates transcription, but genome-wide evidence of this interdependence is lacking. Here, we applied an improved OG-sequencing approach reducing artificial background oxidation and RNA-sequencing to correlate genome-wide distribution of OG with gene transcription in OGG1 and/or MUTYH-deficient cells. Our data identified moderate enrichment of OG in the genome that is mainly dependent on the genomic context and not affected by DNA glycosylase-initiated repair. Interestingly, no association was found between genomic OG deposition and gene expression changes upon loss of OGG1 and MUTYH. Regardless of DNA glycosylase activity, OG in promoter regions correlated with expression of genes related to metabolic processes and damage response pathways indicating that OG functions as a cellular stress sensor to regulate transcription. Our work provides novel insights into the mechanism underlying transcriptional regulation by OG and DNA glycosylases OGG1 and MUTYH and suggests that oxidative DNA damage accumulation and its repair utilize different pathways.http://www.sciencedirect.com/science/article/pii/S2213231724004397
spellingShingle Tobias Obermann
Teri Sakshaug
Vishnu Vignesh Kanagaraj
Andreas Abentung
Mirta Mittelstedt Leal de Sousa
Lars Hagen
Antonio Sarno
Magnar Bjørås
Katja Scheffler
Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
Redox Biology
title Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
title_full Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
title_fullStr Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
title_full_unstemmed Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
title_short Genomic 8-oxoguanine modulates gene transcription independent of its repair by DNA glycosylases OGG1 and MUTYH
title_sort genomic 8 oxoguanine modulates gene transcription independent of its repair by dna glycosylases ogg1 and mutyh
url http://www.sciencedirect.com/science/article/pii/S2213231724004397
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